Natural selection and repeated patterns of molecular evolution following allopatric divergence

  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu  Is a corresponding author
  9. Yun-peng Zhao  Is a corresponding author
  10. Pamela S Soltis  Is a corresponding author
  11. Gane Ka-Shu Wong  Is a corresponding author
  12. Douglas E Soltis  Is a corresponding author
  13. Jenny Xiang  Is a corresponding author
  1. North Carolina State University, United States
  2. University of Florida, United States
  3. Beijing Genomics Institute, China
  4. Chinese Academy of Sciences, China
  5. Zhejiang University, China

Abstract

Although geographic isolation is a leading driver of speciation, the tempo and pattern of divergence at the genomic level remain unclear. We examine genome-wide divergence of putatively single-copy orthologous genes (POGs) in 20 allopatric species/variety pairs from diverse angiosperm clades, with 16 pairs reflecting the classic eastern Asia-eastern North America floristic disjunction. In each pair, >90% of POGs are under purifying selection, and <10% are under positive selection. A set of POGs are under strong positive selection, 14 of which are shared by 10-15 pairs, and one shared by all pairs; 15 POGs are annotated to biological processes responding to various stimuli. The relative abundance of POGs under different selective forces exhibits a repeated pattern among pairs despite an ~10-million-year difference in divergence time. Species divergence times are positively correlated with abundance of POGs under moderate purifying selection, but negatively correlated with abundance of POGs under strong purifying selection.

Data availability

Sequences of ortologous gene families and pairs of POGs sequences used for calculation of Ka and Ks have been submitted to Dryad (https://datadryad.org//). Raw transcriptome data have been submitted to NCBI SRA database with Bioproject number PRJNA508825 and Biosample number from SAMN10534244 to SAMN10534283 (Supplementary File 11).

The following data sets were generated

Article and author information

Author details

  1. Yibo Dong

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Shichao Chen

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shifeng Cheng

    Beijing Genomics Institute, Shenzhen, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Wenbin Zhou

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qing Ma

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Zhiduan Chen

    State Key Laboratory of Systematic and Evolutionary Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Cheng-Xin Fu

    Laboratory of Systematic & Evolutionary Botany and Biodiversity, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Xin Liu

    Beijing Genomics Institute, Shenzen, China
    For correspondence
    liuxin@genomics.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Yun-peng Zhao

    Laboratory of Systematic & Evolutionary Botany and Biodiversity, Zhejiang University, Hangzhou, China
    For correspondence
    ypzhao913@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  10. Pamela S Soltis

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    For correspondence
    psoltis@flmnh.ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Gane Ka-Shu Wong

    Beijing Genomics Institute, Shenzen, China
    For correspondence
    gane@ualberta.ca
    Competing interests
    The authors declare that no competing interests exist.
  12. Douglas E Soltis

    Florida Museum of Natural History, University of Florida, Gainesville, United States
    For correspondence
    dsoltis@ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
  13. Jenny Xiang

    Department of Plant and Microbial Biology, North Carolina State University, Raleigh, United States
    For correspondence
    jenny_xiang@ncsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9016-0678

Funding

National Science Foundation (DEB-442161)

  • Yibo Dong
  • Wenbin Zhou
  • Jenny Xiang

National Science Foundation (DEB-442280)

  • Shichao Chen
  • Pamela S Soltis
  • Douglas E Soltis

National Science Foundation of China (IOS-024629)

  • Shichao Chen
  • Yun-peng Zhao

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Daniel J Kliebenstein, University of California, Davis, United States

Version history

  1. Received: January 15, 2019
  2. Accepted: August 1, 2019
  3. Accepted Manuscript published: August 2, 2019 (version 1)
  4. Version of Record published: September 13, 2019 (version 2)
  5. Version of Record updated: September 20, 2019 (version 3)
  6. Version of Record updated: January 17, 2020 (version 4)

Copyright

© 2019, Dong et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,237
    views
  • 509
    downloads
  • 18
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Yibo Dong
  2. Shichao Chen
  3. Shifeng Cheng
  4. Wenbin Zhou
  5. Qing Ma
  6. Zhiduan Chen
  7. Cheng-Xin Fu
  8. Xin Liu
  9. Yun-peng Zhao
  10. Pamela S Soltis
  11. Gane Ka-Shu Wong
  12. Douglas E Soltis
  13. Jenny Xiang
(2019)
Natural selection and repeated patterns of molecular evolution following allopatric divergence
eLife 8:e45199.
https://doi.org/10.7554/eLife.45199

Share this article

https://doi.org/10.7554/eLife.45199

Further reading

    1. Evolutionary Biology
    Deng Wang, Yaqin Qiang ... Jian Han
    Research Article

    Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.

    1. Biochemistry and Chemical Biology
    2. Evolutionary Biology
    Foteini Karapanagioti, Úlfur Águst Atlason ... Sebastian Obermaier
    Research Article

    The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.